Cognitive and motivational deficits together with prefrontal oxidative stress in a mouse model for neuropsychiatric illness

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 30, 2013, Pages 12462-12467

  Johnson, Alexander W ^a   Jaaro Peled, Hanna ^b   Shahani, Neelam ^b   Sedlak, Thomas W ^b   Zoubovsky, Sandra ^b   Burruss, Daniel ^b   Emiliani, Francesco ^b   Sawa, Akira ^b   Gallagher, Michela ^b  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Cognition; Depression; Orbitofrontal cortex

Indexed keywords

DISRUPTED IN SCHIZOPHRENIA 1 PROTEIN; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; PROTEIN; PROTEIN SIAH; UNCLASSIFIED DRUG;

ADAPTIVE BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; EXPECTANCY; GENE EXPRESSION; GOAL ATTAINMENT; LEARNING; MALE; MENTAL DISEASE; MOTIVATION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; REINFORCEMENT; SOCIAL BEHAVIOR; SOCIAL INTERACTION; STATE DEPENDENT LEARNING; STIMULUS RESPONSE; TASK PERFORMANCE;

COGNITION; DEPRESSION; ORBITOFRONTAL CORTEX;

ANIMALS; COGNITION DISORDERS; MENTAL DISORDERS; MICE; MICE, INBRED C57BL; MOTIVATION; OXIDATIVE STRESS; PREFRONTAL CORTEX; SOCIAL BEHAVIOR;

EID: 84880679755     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1307925110     Document Type: Article

References (50)

1. Baaré WF, et al. (1999) Volumetric analysis of frontal lobe regions in schizophrenia: Relation to cognitive function and symptomatology. Biol Psychiatry 45(12):1597-1605.
2. Hoff AL, Riordan H, O'Donnell DW, Morris L, DeLisi LE (1992) Neuropsychological functioning of first-episode schizophreniform patients. Am J Psychiatry 149(7): 898-903.
3. Drevets WC, Price JL, Furey ML (2008) Brain structural and functional abnormalities in mood disorders: Implications for neurocircuitry models of depression. Brain Struct Funct 213(1-2):93-118.
4. Lesh TA, Niendam TA, Minzenberg MJ, Carter CS (2011) Cognitive control deficits in schizophrenia: Mechanisms and meaning. Neuropsychopharmacology 36(1):316-338.
5. Murrough JW, Iacoviello B, Neumeister A, Charney DS, Iosifescu DV (2011) Cognitive dysfunction in depression: Neurocircuitry and new therapeutic strategies. Neurobiol Learn Mem 96(4):553-563.
6. Price JL, Drevets WC (2010) Neurocircuitry of mood disorders. Neuropsychopharmacology 35(1):192-216.
7. Treadway MT, Zald DH (2011) Reconsidering anhedonia in depression: Lessons from translational neuroscience. Neurosci Biobehav Rev 35(3):537-555.
8. Insel T, et al. (2010) Research domain criteria (RDoC): Toward a new classification framework for research on mental disorders. Am J Psychiatry 167(7):748-751.
9. Beasley CL, Zhang ZJ, Patten I, Reynolds GP (2002) Selective deficits in prefrontal cortical GABAergic neurons in schizophrenia defined by the presence of calciumbinding proteins. Biol Psychiatry 52(7):708-715.
10. Fung SJ, et al. (2010) Expression of interneuron markers in the dorsolateral prefrontal cortex of the developing human and in schizophrenia. Am J Psychiatry 167(12): 1479-1488.
11. Sibille E, Morris HM, Kota RS, Lewis DA (2011) GABA-related transcripts in the dorsolateral prefrontal cortex in mood disorders. Int J Neuropsychopharmacol 14(6): 721-734.
12. Behrens MM, et al. (2007) Ketamine-induced loss of phenotype of fast-spiking interneurons is mediated by NADPH-oxidase. Science 318(5856):1645-1647.
13. Maes M, Galecki P, Chang YS, Berk M (2011) A review on the oxidative and nitrosative stress (O&NS) pathways in major depression and their possible contribution to the (neuro)degenerative processes in that illness. Prog Neuropsychopharmacol Biol Psychiatry 35(3):676-692.
14. Steullet P, et al. (2010) Redox dysregulation affects the ventral but not dorsal hippocampus: Impairment of parvalbumin neurons, gamma oscillations, and related behaviors. J Neurosci 30(7):2547-2558.
15. Yao JK, Keshavan MS (2011) Antioxidants, redox signaling, and pathophysiology in schizophrenia: An integrative view. Antioxid Redox Signal 15(7):2011-2035.
16. Maes M, et al. (2009) Increased 8-hydroxy-deoxyguanosine, a marker of oxidative damage to DNA, in major depression and myalgic encephalomyelitis /chronic fatigue syndrome. Neuroendocrinol Lett 30(6):715-722.
17. Brandon NJ, Sawa A (2011) Linking neurodevelopmental and synaptic theories of mental illness through DISC1. Nat Rev Neurosci 12(12):707-722.
18. Jaaro-Peled H, et al. (2009) Neurodevelopmental mechanisms of schizophrenia: Understanding disturbed postnatal brain maturation through neuregulin-1-ErbB4 and DISC1. Trends Neurosci 32(9):485-495.
19. Blackwood DH, et al. (2001) Schizophrenia and affective disorders-cosegregation with a translocation at chromosome 1q42 that directly disrupts brain-expressed genes: Clinical and P300 findings in a family. Am J Hum Genet 69(2):428-433.
20. Shen S, et al. (2008) Schizophrenia-related neural and behavioral phenotypes in transgenic mice expressing truncated Disc1. J Neurosci 28(43):10893-10904.
21. Hikida T, et al. (2007) Dominant-negative DISC1 transgenic mice display schizophrenia-associated phenotypes detected by measures translatable to humans. Proc Natl Acad Sci USA 104(36):14501-14506.
22. Jaaro-Peled H, Ayhan Y, Pletnikov MV, Sawa A (2010) Review of pathological hallmarks of schizophrenia: Comparison of genetic models with patients and nongenetic models. Schizophr Bull 36(2):301-313.
23. Ayhan Y, et al. (2011) Differential effects of prenatal and postnatal expressions of mutant human DISC1 on neurobehavioral phenotypes in transgenic mice: Evidence for neurodevelopmental origin of major psychiatric disorders. Mol Psychiatry 16(3): 293-306.
24. Jaaro-Peled H, et al. (2013) Subcortical dopaminergic deficits in a DISC1 mutant model: A study in direct reference to human molecular brain imaging. Hum Mol Genet 22(8):1574-1580.
25. Dias R, Robbins TW, Roberts AC (1996) Primate analogue of the Wisconsin Card Sorting Test: Effects of excitotoxic lesions of the prefrontal cortex in the marmoset. Behav Neurosci 110(5):872-886.
26. Rygula R, Walker SC, Clarke HF, Robbins TW, Roberts AC (2010) Differential contributions of the primate ventrolateral prefrontal and orbitofrontal cortex to serial reversal learning. J Neurosci 30(43):14552-14559.
27. O'Doherty J, Critchley H, Deichmann R, Dolan RJ (2003) Dissociating valence of outcome from behavioral control in human orbital and ventral prefrontal cortices. J Neurosci 23(21):7931-7939.
28. Boulougouris V, Dalley JW, Robbins TW (2007) Effects of orbitofrontal, infralimbic and prelimbic cortical lesions on serial spatial reversal learning in the rat. Behav Brain Res 179(2):219-228.
29. Johnson AW, et al. (2010) Localized disruption of Narp in medial prefrontal cortex blocks reinforcer devaluation performance. Learn Mem 17(12):620-626.
30. Izquierdo A, Suda RK, Murray EA (2004) Bilateral orbital prefrontal cortex lesions in rhesus monkeys disrupt choices guided by both reward value and reward contingency. J Neurosci 24(34):7540-7548.
31. Holland PC, Gallagher M (2004) Amygdala-frontal interactions and reward expectancy. Curr Opin Neurobiol 14(2):148-155.
32. Johnson AW, Gallagher M (2011) Greater effort boosts the affective taste properties of food. Proc Biol Sci 278(1711):1450-1456.
33. Hodos W (1961) Progressive ratio as a measure of reward strength. Science 134(3483): 943-944.
34. Sclafani A (2006) Sucrose motivation in sweet "sensitive" (C57BL/6J) and "subsensitive" (129P3/J) mice measured by progressive ratio licking. Physiol Behav 87(4):734-744.
35. Ward RD, Simpson EH, Kandel ER, Balsam PD (2011) Modeling motivational deficits in mouse models of schizophrenia: Behavior analysis as a guide for neuroscience. Behav Processes 87(1):149-156.
36. Kaidanovich-Beilin O, Lipina T, Vukobradovic I, Roder J, Woodgett JR (2011) Assessment of social interaction behaviors. J Vis Exp 48:2473-2477.
37. Moy SS, et al. (2004) Sociability and preference for social novelty in five inbred strains: An approach to assess autistic-like behavior in mice. Genes Brain Behav 3(5):287-302.
38. Smith DR, Burruss DR, Johnson AW (2009) An assessment of olfaction and responses to novelty in three strains of mice. Behav Brain Res 201(1):22-28.
39. Hara MR, et al. (2005) S-nitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding. Nat Cell Biol 7(7):665-674.
40. Tristan C, Shahani N, Sedlak TW, Sawa A (2011) The diverse functions of GAPDH: Views from different subcellular compartments. Cell Signal 23(2):317-323.
41. Arnsten AF (2011) Prefrontal cortical network connections: Key site of vulnerability in stress and schizophrenia. Int J Dev Neurosci 29(3):215-223.
42. Lewis DA, Sweet RA (2009) Schizophrenia from a neural circuitry perspective: Advancing toward rational pharmacological therapies. J Clin Invest 119(4):706-716.
43. Wallis JD (2007) Orbitofrontal cortex and its contribution to decision-making. Annu Rev Neurosci 30:31-56.
44. Valentin VV, Dickinson A, O'Doherty JP (2007) Determining the neural substrates of goal-directed learning in the human brain. J Neurosci 27(15):4019-4026.
45. Kouneiher F, Charron S, Koechlin E (2009) Motivation and cognitive control in the human prefrontal cortex. Nat Neurosci 12(7):939-945.
46. Haber SN, Fudge JL, McFarland NR (2000) Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum. J Neurosci 20(6): 2369-2382.
47. Sesack SR, Grace AA (2010) Cortico-Basal Ganglia reward network: Microcircuitry. Neuropsychopharmacology 35(1):27-47.
48. Porteous DJ, Millar JK, Brandon NJ, Sawa A (2011) DISC1 at 10: Connecting psychiatric genetics and neuroscience. Trends Mol Med 17(12):699-706.
49. Do KQ, Cabungcal JH, Frank A, Steullet P, Cuenod M (2009) Redox dysregulation, neurodevelopment, and schizophrenia. Curr Opin Neurobiol 19(2):220-230.
50. Glowinski J, Iversen LL (1966) Regional studies of catecholamines in the rat brain. I. The disposition of [3H]norepinephrine, [3H]dopamine and [3H]dopa in various regions of the brain. J Neurochem 13(8):655-669.